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Home based neuromuscular electrical stimulation as

a new rehabilitative strategy for severely disabled
patients with chronic obstructive pulmonary disease
(COPD)
J A Neder, D Sword, S A Ward, E Mackay, L M Cochrane and C J Clark

Thorax 2002;57;333-337
doi:10.1136/thorax.57.4.333

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333

ORIGINAL ARTICLE

Home based neuromuscular electrical stimulation as a

new rehabilitative strategy for severely disabled patients
with chronic obstructive pulmonary disease (COPD)
J A Neder, D Sword, S A Ward, E Mackay, L M Cochrane, C J Clark
.............................................................................................................................

Thorax 2002;57:333–337

See end of article for
authors’ affiliations
.......................
Correspondence to:
Dr C J Clark, Department
of Respiratory Medicine,
Hairmyres Hospital, East
Kilbride, Glasgow
G75 8RG, UK;
chris.clark@laht.scot.nhs.uk
Revised version received
13 December 2001
Accepted for publication
9 January 2002
.......................
Background: Passive training of specific locomotor muscle groups by means of neuromuscular electri-
cal stimulation (NMES) might be better tolerated than whole body exercise in patients with severe
chronic obstructive pulmonary disease (COPD). It was hypothesised that this novel strategy would be
particularly effective in improving functional impairment and the consequent disability which character-
ises patients with end stage COPD.
Methods: Fifteen patients with advanced COPD (nine men) were randomly assigned to either a home
based 6 week quadriceps femoris NMES training programme (group 1, n=9, FEV1=38.0 (9.6)% of
predicted) or a 6 week control period before receiving NMES (group 2, n=6, FEV1=39.5 (13.3)% of
predicted). Knee extensor strength and endurance, whole body exercise capacity, and health related
quality of life (Chronic Respiratory Disease Questionnaire, CRDQ) were assessed.
Results: All patients were able to complete the NMES training programme successfully, even in the
presence of exacerbations (n=4). Training was associated with significant improvements in muscle
function, maximal and endurance exercise tolerance, and the dyspnoea domain of the CRDQ
(p<0.05). Improvements in muscle performance and exercise capacity after NMES correlated well with
a reduction in perception of leg effort corrected for exercise intensity (p<0.01).
Conclusions: For severely disabled COPD patients with incapacitating dyspnoea, short term electrical
stimulation of selected lower limb muscles involved in ambulation can improve muscle strength and
endurance, whole body exercise tolerance, and breathlessness during activities of daily living.

E
xercise intolerance is a hallmark of chronic obstructive
pulmonary disease (COPD) and is commonly associated
with reduced quality of life and increased utilisation of
healthcare resources.1 Traditionally, exercise intolerance has
been ascribed to respiratory mechanical and/or pulmonary gas
exchange disturbances and their perceptual consequences
which are manifest mainly as breathlessness (dyspnoea),
especially on exertion.2
It is increasingly clear, however, that a chronic progressively
sedentary lifestyle generally ensues, a process long recognised
as the “dyspnoea spiral”.3 Evidence has accumulated to
suggest that, as part of this vicious cycle, deconditioning of
skeletal muscle occurs which contributes significantly to exer-
cise intolerance in this patient population.4–7 Exercise training,
typically as a component of pulmonary rehabilitation, has
been shown to improve exercise tolerance in COPD.8 However,
physical training of very severe patients, such as those who
present with intense breathlessness at rest or on minimum
exertion, can be particularly difficult. In this population,
training has been shown to be associated with less consistent
benefits than those characteristically found in patients with
mild to moderate dyspnoea.9 10
We therefore propose that passive stimulation of locomotor
muscle groups by neuromuscular electrical stimulation
(NMES) may provide an alternative approach for improving
physical capacity in severely compromised patients with
COPD who present with incapacitating dyspnoea. Application
of NMES has been consistently associated with increased
mass, strength, and endurance of both normally and
abnormally innervated muscles in a range of pathological
conditions.11–13 Although experience with NMES in patients
with skeletal muscle dysfunction secondary to congestive
heart failure is accruing,14–17 the efficacy of this technique has
yet to explored in COPD.
Using a randomised controlled trial, the objective of the
present investigation was therefore to evaluate the potential
for NMES to improve peripheral muscle function, and to
evaluate the impact of any such changes on exercise tolerance
and health related quality of life of patients with advanced
COPD.
METHODS
Patients
Fifteen patients (nine men) with a clinical and functional
diagnosis of COPD comprised the study group. All subjects
presented with moderate to severe ventilatory impairment
(forced expiratory volume in 1 second (FEV1) <50% pre-
dicted) and incapacitating breathlessness according to the
Medical Research Council scale18—that is, scores of 4 (“I stop
for breath after walking 100 yards or after a few minutes on
the level”) or 5 (“I am too breathless to leave the house”).
Inclusion criteria were absence of associated locomotor or
neurological conditions, and disease stability as indicated by
no change in medication dosage or exacerbation of symptoms
in the preceding 4 weeks.
Before participating in the study all the procedures and any
associated risks were described in detail to the patients. Writ-
ten informed consent (as approved by the institutional medi-
cal ethics committee) was then obtained from each patient.
Design and procedures
This was a prospective randomised controlled study. The
patients were referred from the respiratory clinic of Hairmyres
Hospital by two investigators who were blind to the order of
patient allocation. Patients were randomised to group 1 who
initially received NMES (n=9) or to group 2 who received
NMES after a control period (n=6). Group 1 was evaluated

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334
twice (before and after NMES) and group 2 was assessed three
times (before and after the 6 week control period and after a
further 6 week period of NMES). The NMES training period
was consistent with the training duration shown to be effec-
tive in previous studies of NMES.11 12 15 17
Each evaluation consisted of a 3 day protocol which
included: (1) a questionnaire based evaluation of the health
related quality of life, body composition assessment, pulmo-
nary function tests, and a maximum incremental cardiopul-
monary exercise test (CPET) (day 1); (2) a knee strength and
endurance evaluation by isokinetic dynamometry (day 2); and
(3) an endurance constant work rate CPET to the limit of tol-
erance (day 3).
Measurements
Health related quality of life
The Chronic Respiratory Questionnaire19 was administered to
obtain an index of the health related quality of life. In this
instrument four domains are measured: “dyspnoea” (using
self-selected daily activities), “fatigue”, “mastery”, and “emo-
tional function”. Each domain has 4–7 items scored on a scale
of 1–7. A change of 0.5 in the arithmetic mean score per
domain has been shown to be related to a minimally
important difference in general health status.19
Body composition
Fat-free mass (FFM) was measured by the bioelectrical
impedance method (Bodystat-500; Bodystat Ltd, Douglas,
UK). Impedance measurements were performed on the right
side with subjects supine and with their limbs slightly apart
from the trunk. FFM was calculated using a validated patient
specific regression equation20 from Ht2/Res and total body
mass and expressed as a percentage of ideal body weight.
Pulmonary function tests
Spirometric tests were performed using the 2130D Sensor-
Medics spirometer (SensorMedics Corp, CA, USA), flow being
measured with a calibrated pneumotachograph. The subjects
completed at least three acceptable maximal forced expiratory
manoeuvres before and 20 minutes after 200 µg inhaled salb-
utamol. Maximal voluntary ventilation (MVV, l/min) was esti-
mated from the product FEV1 (l) × 37.5. A computer based
automated system (VMax 22 System, SensorMedics Corp)
was used to measure static lung volumes by the “breath by
breath” nitrogen washout technique and lung diffusion
capacity for carbon monoxide (transfer factor) by the
modified Krogh technique (single breath).
Cardiopulmonary exercise tests
Exercise tests were performed on an electromagnetically
braked cycle ergometer with the subjects maintaining a
pedalling frequency of 50 (5) rpm. Each subject initially
underwent a symptom limited incremental exercise test (5 W/
min). On a different day each subject completed a constant
work rate test to the limit of tolerance (Tlim), with the work
rate being maintained constant at 80–90% of the peak work
rate obtained in the incremental test.21
During the exercise tests respired O2 and CO2 concentrations
and respired flow were monitored continuously by calibrated
rapidly responding gas analysers and an anemometer, respec-
tively (VMax 229 System, SensorMedics Corp). Pulmonary
oxygen uptake (V ~ O2, l/min STPD) and minute ventilation (V ~ E,
l/min BTPS) were derived breath by breath and expressed as
15 s stationary averages. Heart rate (HR, bpm) was derived
beat by beat using the R–R interval from a 12-lead electrocar-
diogram, and oxyhaemoglobin saturation (SaO2) by pulse oxi-
metry. Subjects were also asked to rate “shortness of breath”
or “leg effort” each minute in an alternating sequence using
the Borg category ratio scale (0–10). The peak V ~ O2 values on
the incremental test were compared with those predicted by
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Neder, Ward, Sword, et al
Table 1 Anthropometric and lung function
characteristics at baseline
Variable Group 1 (n=9) Group 2 (n=6)
Age (years) 66.6 (7.7) 65.0 (5.4)
Height (cm) 157.0 (9.6) 149.2 (5.2)
Weight (kg) 61.2 (17.5) 57.3 (20.7)
Body mass index (kg/m2) 24.8 (6.9) 25.6 (8.8)
Fat-free mass (% ideal weight) 67.3 (9.8) 68.9 (10.9)
FEV1 (l) 0.94 (0.19) 0.97 (0.34)
FEV1 (% predicted) 38.0 (9.6) 39.5 (13.3)
FVC (% predicted) 54.0 (13.3) 57.2 (11.3)
FEV1/FVC 0.49 (0.11) 0.49 (0.08)
RV (% predicted) 154.2 (41.8) 184.0 (26.1)
TLCO (% predicted) 56.1 (15.8) 49.5 (12.6)
FEV1 = forced expiratory volume in 1 second; FVC = forced vital
capacity; RV = residual volume (by helium dilution), TLCO = single
breath transfer factor for carbon monoxide.
Neder et al, taking into consideration sedentariness, sex, age,
weight, and height.22
Peripheral muscle strength and endurance
Concentric contractions of the quadriceps femoris (knee
extension) of the dominant leg were evaluated using an isoki-
netic dynamometer (KinCom, Cybex, Chattanooga, NY,
USA).23 All patients performed: (1) a maximum isokinetic
strength test with three movements tested at an angular
velocity of 70°/s separated by 1–3 minutes rest (peak torque in
N.m); (2) a maximal isometric test in which the subjects were
asked to sustain the lever arm at 40° for 5 seconds while the
force applied was instantaneously recorded (mean force in N);
and (3) an endurance test for 1 minute in which the subjects
were asked to perform the maximum possible number of con-
tractions at an angular velocity of 70°/s during this time frame
(total work in J, mean power in W, and a fatigue index
expressed as the % ratio between the work performed in the
three last and three initial contractions).
Training protocol
The NMES training protocol used was based on that of Kots,24
later modified by Selkowitz.25 A portable, user friendly, dual
channel NME stimulator was used (Respond Select, Empi Inc,
South Dakota, USA). The following training protocol was cho-
sen in order to minimise the effects of fatigue on muscle con-
tractility:
(a) symmetrical biphasic square pulsed current at 50 Hz;
(b) duty cycle: 2 s on and 18 s off (10%) in the first week, 5 s
on and 25 s off (17%) in the second week, and 10 s on and 30 s
off (25%) thereafter;
(c) pulses 300–400 µs wider using the highest tolerable ampli-
tude (10–20 mA at the start of the training session increasing
up to 100 mA).
This training protocol was applied in each leg (15 minutes
in the first week and 30 minutes thereafter), in sequence, five
times per week for 6 weeks (a total of 30 sessions). During the
NMES application the patient’s back was fully supported but
the limb receiving treatment was left hanging unsupported.
In order to familiarise the patients with the equipment and
to detect possible side effects, the NMES training protocol was
initially applied under the guidance of a qualified and experi-
enced physiotherapist in an outpatient hospital setting (first
week). A “user diary” was completed daily in the home based
training phase to include the patient’s subjective impressions
during and between the training sessions. In addition, the
same physiotherapist responsible for the training assessed
compliance at a weekly visit to the patient’s home, during
which she adjusted the stimulator settings and checked a hid-
den system recording clock which recorded cumulative time of
usage.
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Home based rehabilitation for severely disabled patients with COPD 335

Table 2 Whole body exercise tolerance and peripheral muscle strength in patients who received NMES (group 1, n=9)
and controls (group 2, n=6)
Baseline Follow up

Difference between Difference between means

Group 1 Group 2 means (95% CI) Group 1 Group 2 (95% CI)

Maximal exercise
Power (W) 24 (15) 23 (17) 1 (–7 to 9) 36 (12) 27 (18) 9 (−5 to 23)
V̇O2 (l/min) 0.60 (0.15) 0.53 (0.10) 0.07 (–0.08 to 0.22) 0.72 (0.16) 0.59 (0.19) 0.13 (0.03 to 0.23)*
LE/V̇O2 11.3 (5.3) 11.1 (4.1) 0.2 (–1.2 to 1.6) 7.9 (3.0) 10.7 (4.1) –2.8 (–5.0 to –0.6)*
BL/V̇O2 13.5 (2.9) 13.7 (3.8) –0.2 (–2.9 to 2.5) 9.1 (2.7) 14.1 (3.3) –5.0 (–11.2 to 1.2)

Endurance exercise
Time (min) 4.5 (2.1) 3.9 (1.6) 0.6 (–2.3 to 3.5) 8.4 (2.0) 3.4 (1.8) 5.0 (2.9 to 7.1)*
LE/Tlim 2.17 (0.31) 2.20 (0.35) –0.03 (–0.41 to 0.35) 0.94 (0.34) 2.15 (0.48) –1.19 (–1.78 to −0.60)*
BL/Tlim 2.95 (0.49) 3.11 (0.48) –0.16 (–0.85 to 0.53) 2.06 (0.28) 3.15 (0.29) –1.09 (–2.03 to 0.15)

Muscle strength
Peak torque (N.m) 64.4 (32.3) 54.5 (16.2) 9.9 (–10.7 to 30.5) 91.8 (29.3) 59.7 (6.8) 32.1 (6.1 to 58.1)*
Fatigue index (%) 113.7 (35.2) 96.5 (19.1) 17.2 (–2.1 to 36.5) 74.9 (38.8) 98.1 (13.1) –23.2 (–42.5 to –3.9)*
Mean isometric force (N) 156.8 (53.6) 150.5 (60.4) 6.3 (–26.9 to 39.5) 185.5 (54.6) 164.3 (71.4) 21.2 (–10.8 to 53.2)

V̇O2 = oxygen uptake; V̇E = minute ventilation; LE = leg effort; BL = breathlessness,Tlim = time to the limit of tolerance of constant work rate exercise.
*p<0.05.

Statistical analysis define the associations between variables. The probability of a

Mean (SD) values were obtained for subjects in both groups. type I error was established at 0.05 for all tests.
Between group differences at baseline and after 6 weeks were
assessed by an unpaired Student’s t test; mean differences and
their 95% confidence intervals are reported for the main out- RESULTS
comes. In addition, the data following NMES in patients in Baseline characteristics
group 2 were compared with baseline values using a paired t No significant differences were found between the groups in
test. Product-moment correlation (Pearson) was used to anthropometric and lung function variables at baseline (table

A 180 B
180
140
Peak torque (N.m)

140
Fatigue index (%)

100
100

60 60

20 20
Baseline 6 week* 12 week* Baseline 6 week* 12 week*
C 11 D
10
900
Peak oxygen uptake (ml/min)

9
8
7
Tlim (min)

700
6
5
500 4
3
2
300 1
Baseline 6 week* 12 week* Baseline 6 week* 12 week*
Figure 1 Individual values for (A) maximal knee isokinetic strength (peak torque), (B) endurance (fatigue index), (C) maximum (peak oxygen
uptake), and (D) endurance (time, Tlim) exercise capacities at baseline and 6 and 12 weeks. Note that while patients in group 1 (n=9, solid
lines) received NMES after enrolment, those in group 2 (n=6, dashed lines) were submitted to a control period before receiving NMES.
*p<0.05 for all variables (group 1 v group 2 after 6 weeks and in group 2 at 12 weeks v baseline).

www.thoraxjnl.com
 Downloaded from thorax.bmjjournals.com on 28 October 2005
336
1). The tolerance to incremental cycle ergometric tests was
severely reduced in both groups relative to predicted values
(table 2).22
Although breathlessness was the main limiting symptom to
incremental exercise (median 7 (range 4–10)), leg effort was
also an important contributory factor for all patients (5
(3–9)). Both groups had marked reductions in muscle
strength and endurance—for example, peak torque was only
55.8 (20.5)% predicted in group 1 and 61.3 (15.7)% predicted
in group 2.26
Physiological and subjective effects of NMES
All patients were able to complete the training sessions
successfully. Compliance was excellent: all patients completed
their diaries fully and the hidden clock system confirmed that
the NMES system was used for the expected period. While
four patients (two in each group) presented with mild exacer-
bations of COPD during the training period, they were able to
continue the NMES training safely during these events. There
were no reports in the patients’ diaries of any side effects of
NMES, such as pain or discomfort.
Peripheral muscle strength and endurance
Significant mean differences in maximal isokinetic strength
(peak torque) and muscle fatigue were found between the two
groups (table 2 and fig1A and B). Although we did find trends
for improvement after NMES in isometric mean force and
other indices of muscle endurance such as total work and
mean power, they did not reach statistical significance
(p>0.05). Peak torque and muscle fatigue after NMES in
patients in group 2 were also significantly higher than those
found at baseline (fig 1A and B).
Whole body incremental and endurance exercise
Application of NMES was associated with an enhanced toler-
ance to whole body incremental exercise, as inferred from
symptom limited peak V ~ O2 and endurance exercise (table 2
and fig 1C and D). The most striking effects, however, were
found in the endurance capacity: the percentage increase
((post – pre)/pre × 100) in Tlim following NMES training was
~ O2 (84.5 (21.3)% v 16.3
substantially larger than that for peak V
(8.1)%; p<0.01). Similarly, values for peak V ~ O2 and Tlim were
significantly higher after NMES than at baseline in patients in
group 2 (fig 1C and D)
Health related quality of life
NMES training was associated with beneficial changes in the
“dyspnoea” domain of the quality of life questionnaire19 with
a mean difference between groups 1 and 2 after 6 weeks of 1.2
(95% CI 0.4 to 2.0). No between group differences were
observed in “fatigue”, “emotional function”, and “mastery”
domains. In addition, in group 2 the mean scores for dyspnoea
after NMES were significantly improved compared with base-
line (mean difference 1.4 (95% CI 0.5 to 2.3); p<0.05).
Correlates of improvement after NMES
No significant relationship was found between the magnitude
of training related improvement and the resting or exercise
baseline data. However, improvements in muscle function
(peak torque) and exercise tolerance (Tlim) correlated signifi-
cantly with reduced leg effort adjusted for post-training
changes in exercise duration (constant work rate test) (R =
–0.77 and –0.74, respectively; p<0.01).
DISCUSSION
This study constitutes, we believe, the first description of the
effects of NMES on peripheral muscle function, whole body
exercise tolerance, and health related quality of life in patients
with advanced COPD. Using a 6 week home based NMES
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Neder, Ward, Sword, et al
training programme, we were able to enhance patients’ func-
tional capacity which was reflected in an improvement in self-
reported daily dyspnoea. These preliminary findings suggest
that NMES can be a safe and effective strategy for rehabilitat-
ing patients with severe COPD who present with incapacitat-
ing breathlessness.
The major advantage of NMES over conventional exercise
training in patients with COPD is the virtual absence of venti-
latory stress during passive exercise, reflecting the smaller
muscle mass involved. Our patients were therefore comfort-
ably able to cope with a training regimen which, if provided by
voluntary dynamic contractions, would be demanding and
probably not tolerable. In fact, from the patients’ diaries there
was a consistent view that the associated sensations were not
painful or uncomfortable, which emphasises the importance
of including some days of familiarisation and a progressive
training scheme. In this context, we also found that four
patients were able to maintain their NMES training even in
the presence of an acute exacerbation. This finding raises the
hypothesis that NMES could be valuable for ameliorating the
marked decrease in muscle strength (and mass) which is fre-
quently observed following acute exacerbations of COPD.27
Our data are consistent with growing evidence that NMES
can be safely and effectively used in patients with skeletal
muscle function deficit and exercise intolerance secondary to
systemic diseases.14–17 Quittan et al, for example, have described
substantial gains in muscle strength and exercise tolerance
after NMES in patients with congestive heart failure which
has been confirmed by others.14–17 These positive effects of
NMES are likely to be similar to those morphological changes
described by Maltais and colleagues9 in patients with COPD
who were submitted to conventional endurance training.
Using a comprehensive range of outcome measures, our study
showed a reduction in leg effort for a given level of exercise
after NMES training (table 2) which would be consistent with
this view. Further morphological studies after NMES training,
however, will be required to confirm this hypothesis.
It is also interesting to note that the beneficial changes in
muscle function found in this study could be translated into
more general benefit. A recent position statement on
pulmonary rehabilitation28 recommends assessment of the
efficacy of treatment using the World Health Organisation’s
description29 of illness impact across three domains—
impairment (skeletal muscle function), activity limitation
(exercise tolerance), and participation restriction (chronic
dyspnoea)—and our NMES training programme achieved
improvements in all of them.
The major limitation of this study relates to its small sample
size. It is likely that the study lacked statistical power to
unravel the full benefits of the intervention. In fact, several of
the outcomes failed to reach statistical significance despite
clear trends towards improvement: this was particularly true
for some indices of muscle endurance and, interestingly, the
amount of breathlessness corrected for exercise intensity
(table 2). In this context, the study should be viewed as an
initial investigation of the feasibility and short term efficacy of
NMES. Further randomised controlled trials using larger
samples with a longer follow up period are clearly warranted.
We were also not able to re-evaluate patients in group 1 after
NMES—that is, this was not a true crossover study. We
considered it unethical to submit these frail patients to an
additional period of physical detraining followed by a
demanding period of retesting, but offered all patients access
to our formal pulmonary rehabilitation programme on
completion of active NMES treatment on the basis that any
improvement, if our hypothesis was correct, should be
consolidated. In addition, it would be interesting to compare
NMES alone or in addition to mild resistive (weight)
training30 with conventional rehabilitation programmes, par-
ticularly in this specific group of severe patients. Furthermore,
a formal cost effectiveness analysis is necessary before the
 Downloaded from thorax.bmjjournals.com on 28 October 2005
Home based rehabilitation for severely disabled patients with COPD
widespread use of NMES can be recommended. Our initial
impression of the cost outlay per patient device is encourag-
ing: reliable, robust stimulators are currently commercially
available for £200–300 and, once issues of bulk purchase are
taken into account, this figure could perhaps be reduced fur-
ther.
In conclusion, a 6 week home based neuromuscular electri-
cal stimulation programme has been shown to improve some
markers of skeletal muscle strength and endurance in patients
with severe COPD. These beneficial effects on peripheral mus-
cle function were translated into an improved ability to
perform whole body exercise and were associated with
reduced breathlessness on the activities of daily living. These
preliminary findings need to be confirmed by larger ran-
domised controlled trials.
ACKNOWLEDGEMENTS
The authors are grateful to Mrs J Sullivan, K Fife, D MacFarlane, and
I Johnson (Department of Respiratory Medicine, Hairmyres Hospital)
for their skilful technical assistance.
.....................
Authors’ affiliations
J A Neder, D Sword, S A Ward, E Mackay, L M Cochrane,
C J Clark, Department of Respiratory Medicine, Hairmyres Hospital, East
Kilbride and Centre for Exercise Science and Medicine, Institute of
Biomedical and Life Sciences (IBLS), University of Glasgow, Glasgow, UK
J A Neder was supported by a long term Research Fellowship Grant from
the European Respiratory Society.
REFERENCES
1 National Heart Lung and Blood Institute and World Health
Organisation (NHLBI/WHO). Global strategy for the diagnosis,
management, and prevention of chronic obstructive pulmonary disease.
Am J Respir Crit Care Med 2001;163:1256–76.
2 Dodd DS, Brancatisano T, Engel LA. Chest wall mechanics during
exercise in patients with severe chronic airflow obstruction. Am Rev
Respir Dis 1984;129:33–8.
3 Belman MJ. Exercise in chronic obstructive pulmonary disease. Clin
Chest Med 1986;7:585–97.
4 American Thoracic Society and European Respiratory Society
Statement (ATS/ERS). Skeletal muscle dysfunction in chronic obstructive
pulmonary disease. Am J Respir Crit Care Med 1999;159(suppl):S1–40.
5 Whittom F, Jobin J, Simard P-M, et al. Histochemical and morphological
characteristics of the vastus lateralis muscle in patients with chronic
obstructive pulmonary disease. Med Sci Sports Exerc 1998;30:1467–
74.
6 Gosselink R, Troosters T, Decramer M. Peripheral muscle contributes to
exercise limitation in COPD. Am J Respir Crit Care Med
1996;153:976–80.
7 Sala E, Roca J, Marrades RM, et al. Effects of endurance training on
skeletal muscle bioenergetics in chronic obstructive pulmonary disease.
Am J Respir Crit Care Med 1999;159:1726–34.
8 Lacasse Y, Wong E, Guyatt GH, et al. Meta-analysis of respiratory
rehabilitation in chronic obstructive pulmonary disease. Lancet
1996;348:1115–9.
337
9 Jones DT, Thomson RJ, Sears MR. Physical exercise and resistive
breathing in severe chronic airways obstruction – are they effective? Eur J
Respir Dis 1985;67:159–66.
10 Wedzicha JA, Bestall JC, Garrod R, et al. Randomized controlled trial of
pulmonary rehabilitation in severe chronic obstructive pulmonary disease
patients, stratified with the MRC dyspnoea scale. Eur Respir J
1998;12:363–9.
11 Hainaut K, Duchateau J. Neuromuscular electrical stimulation and
voluntary exercise. Sports Med 1992;14:100–15.
12 Lake DA. Neuromuscular electrical stimulation: on overview and its
application in the treatment of sports injuries. Sports Med
1992;13:320–35.
13 Glaser RM. Functional meuromuscular stimulation: exercise conditioning
of spinal cord injured patients. Int J Sports Med 1994;15:142–8.
14 Maillefert JF, Eicher JC, Walker P, et al. Effects of low-frequency
electrical stimulation of quadriceps and calf muscles in patients with
chronic heart failure. J Cardiopulm Rehabil 1998;18:277–82.
15 Vaquero AF, Chicharro JL, Gil L, et al. Effects of muscle electrical
stimulation on peak V̇O2 in cardiac transplant patients. Int J Sports Med
1998;19:317–22.
16 Quittan M, Sochor A, Wiesinger GF, et al. Strength improvement of
knee extensor muscles in patients with chronic heart failure by
neuromuscular electrical stimulation. Artif Organs 1999;23:432–5.
17 Quittan M, Wiesinger GF, Sturm B, et al. Improvement of thigh muscles
by neuromuscular electrical stimulation in patients with refractory heart
failure: a single-blind, randomized, controlled trial. Am J Phys Med
Rehabil 2001;80:206–14.
18 Fletcher CM (Chairman). Standardised questionnaire on respiratory
symptoms: a statement prepared and approved by the MRC Committee
on the Aetiology of Chronic Bronchitis (MRC breathlessness score). BMJ
1960;2:1665.
19 Guyatt GH, Berman LB, Townsend M, et al. A measure of quality of life
for clinical trials in chronic lung disease. Thorax 1987;42:773–8.
20 Schols AM, Wouters EF, Soeters PB, et al. Body composition by
bioelectrical-impedance analysis compared with deuterium dilution and
skinfold anthropometry in patients with chronic obstructive pulmonary
disease. Am J Clin Nutr 1991;53:421–4.
21 Neder JA, Jones PW, Nery LE, et al. Determinants of the exercise
endurance capacity in patients with COPD: the power-duration
relationship. Am J Respir Crit Care Med 2000;162:497–504.
22 Neder JA, Nery LE, Castelo A, et al. Prediction of metabolic and
cardio-pulmonary responses to maximum cycle ergometry: a randomized
study. Eur Respir J 1999;4:1304–13.
23 Gleeson NP, Mercer TH. The utility of isokinetic dinamometry in the
assessment of human muscle function. Sports Med 1996;21:18–34.
24 Kots JM. Trenirovka myseckoj sily metodon elektrostimulaciji Soobstenie.
Teorija I Praktika Fiziceskoi Kultury 1971;3:64–7.
25 Selkowitz DM. Improvement in isometric strength of the quadriceps
femoris. Phys Ther 1985;65:186–96.
26 Neder JA, Nery LE, Shinzato GT, et al. Reference values for knee
strength and power in nonathletic males and females 20 to 80 years old.
J Orthop Sports Phys Ther 1999;29:116–26.
27 Engelen MP, Schols AM, Lamers RJ, et al. Different patterns of chronic
tissue wasting among patients with chronic obstructive pulmonary
disease. Clin Nutr 1999;18:275–80.
28 Donner CF, Decramer M, eds. Pulmonary rehabilitation. Sheffield:
European Respiratory Society, 2000.
29 World Health Organisation. International classification of functioning,
disabilitiy and health. Geneva: WHO, 2001.
30 Clark CJ, Cochrane LM, Mackay E, et al. Skeletal muscle strength and
endurance in patients with mild COPD and the effects of weight training.
Eur Respir J 2000;15:92–7.
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